HERPETOLOGICAL JOURNAL 21: 219–225, 2011 Reproduction of Xenodon dorbignyi on the north coast of Rio Grande do Sul, Brazil

Roberto Baptista de Oliveira1,2, Gláucia Maria Funk Pontes1,2, Ana Paula Maciel1, Leandro Ribeiro Gomes1,2 & Marcos Di-Bernardo1,2*

1Laboratório de Herpetologia, Museu de Ciências e Tecnologia, Pontifícia Universidade Católica do Rio Grande do Sul, Brazil 2Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Brazil *In memoriam

Information on sexual maturity, reproductive cycle, fecundity and sexual dimorphism of Xenodon dorbignyi was obtained from 537 individuals captured in a 333 ha sand dune area on the north coast of Rio Grande do Sul, Brazil, and from dissection and analysis of gonads of 98 specimens from the same region deposited in scientific collections. Females and males reach sexual maturity at about 260 mm and 220 mm snout–vent length (SVL), respectively. Males reach sexual maturity in their first year, whereas some females mature in their second year. Both sexes reach similar SVL; males have a relatively longer tail, and mature females have a heavier body. Reproduction is seasonal, with vitellogenesis occurring from August to January, mating from August to December, oviposition from November to February, and hatching from January to April. Clutch size varied from three to 10 eggs and was correlated with maternal SVL. The ratio between clutch mass and female total mass varied between 0.19 and 0.42 (>0.30 in 80% of observations). Key words: Dipsadidae, natural history, reproductive cycle, Serpentes, sexual dimorphism, southern Brazil

INTRODUCTION do Sul, gathered from a large number of observations in nature and from dissections of specimens deposited in he life history of an organism is characterized by re- collections. Tproductive mode, reproductive frequency, clutch and litter size, size of newborns and age and size at sexual ma- MATERIALS AND METHODS turity (Pough et al., 2004). As a consequence of different reproductive costs, the age and size at which individuals The northern coast of Rio Grande do Sul is mainly char- mature can vary both inter- and intraspecifically (Parker acterized by a plain of mobile dunes, interposed by small & Plummer, 1987), leading to sexual size dimorphism at humid depressions and patches with scarce vegetation, the adult stage (Shine, 1993). Fecundity is an important mostly Graminae (Waechter, 1985). The climate is tem- determinant for female reproductive success (Bonnet et perate, with mean, minimum and maximum monthly al., 2001; Lourdais et al., 2003), in addition to timing of temperatures ranging between 15.4, 12.2 and 18.3 ºC in oviposition and quality of offspring (e.g. Olsson & Shine, July, and 24.8, 21.3 and 27.6 ºC in February, respectively. 1997; Madsen & Shine, 1998). High reproductive out- Rainfall is almost uniform across the year, with a small put can be limited by environmental, genetic, behavioral, peak during winter and a mean of 1323 mm (Hasenack & physiological and morphological factors (Williams, 1966; Ferraro, 1989). Shine, 1992). Field observations were carried out from July 1998 Xenodon dorbignyi (Duméril, Bibron & Duméril, to June 2004 in a 333 ha area of sand dunes located in 1854) is an oviparous dipsadid snake (tribe Xenodonti- Magistério (30º21'S, 50º17'W), municipality of Balneário ni) distributed in Paraguay, Argentina, Uruguay and the Pinhal. southernmost parts of Brazil, where it occupies open en- Complementary information was gathered from 98 vironments (Gudynas, 1979; Lema, 1994; Tozetti et al., specimens (30 males and 68 females) collected locally 2010). Information on its reproductive biology mostly and deposited in the herpetological collection of the comprises records of clutches, hatchlings born in captivity Museu de Ciências e Tecnologia of Pontifícia Universi- and occasional observations of mating, mainly from pop- dade Católica do Rio Grande do Sul (MCP), Fundação ulations in Uruguay and Argentina (e.g. Orejas-Miranda, Zoobotânica do Rio Grande do Sul (MCN), and Depar- 1966; Gallardo, 1977; Gudynas, 1979; Leitão-de-Araújo, tamento de Zoologia of Universidade Federal do Rio 1978); Pontes & Di-Bernardo (1988) presented the only Grande do Sul (DZUFRGS) (Appendix 1). Specimens reproductive data available for populations from Rio from collections were dissected, recording snout–vent Grande do Sul. length (SVL), tail length (TL), sex, number of eggs or This study presents information about sexual maturity, vitellogenic follicles, size of the larger follicle or egg (in sexual dimorphism, reproductive cycle and fecundity mm), and condition of deferent ducts. Individuals were of Xenodon dorbignyi on the north coast of Rio Grande considered mature when they had vitellogenic follicles

Correspondence: R.B. Oliveira, Laboratório de Herpetologia, Museu de Ciências e Tecnologia, Pontifícia Universidade Católica do Rio Grande do Sul, Av. Ipiranga 6681, 90619-900 Porto Alegre-RS, Brazil. E-mail: [email protected]

219 R.B. Oliveira et al.

larger than 8 mm or eggs in oviducts (females), or when they had convoluted and opaque deferent ducts (males, cf. Shine, 1982). For ambiguous specimens, transverse slices of the median region of the testis were prepared on slides, stained with haematoxilin-eosin and analysed for the presence or absence of spermatozoa. Maturity of live individuals was inferred based on SVL. Sexual dimorphism was evaluated based on 537 live specimens (260 males and 277 females), and on 100 spec- imens (40 males and 60 females) born in captivity from gravid females captured in the study area. All individuals were measured (SVL and TL, using a ruler), weighed (in grams, using Pesola spring scales), and sexed by forced eversion of the hemipenes. The animals were individually marked by branding ventral scales with a burning wire (cf. Di-Bernardo et al., 2007), and released at their site of capture. After the branding process, marks were treated with antiseptic spray and an anaesthetic (benzalkonium chloride plus lidocaine) to avoid infection by pathogens. Only data from the first capture were used. In order to avoid the inclusion of possibly gravid females in the body mass analysis, only data from mature individuals collect- Fig. 1. Seasonal distribution of snout–vent length ed from March to July (out of the reproductive season) of females (above) and males (below) of Xenodon were included. Since the SVL of both mature males and dorbignyi. The stippled line represents the snout–vent females violated the assumptions of equality of variance, length of the smallest mature individual. an adjusted Student’s t-test was used (t') to compare their means (cf. Zar, 1999). Differences in TL and body mass were investigated by comparing their regressions in rela- tion to SVL. The homogeneity of slopes was compared through analyses of variance (ANOVA), and the inter- cepts were compared with each other using covariance analysis (ANCOVA) after ln transformation of data. The vitellogenic period was inferred from the seasonal RESULTS distribution of the larger follicles of dissected females. The mating season was determined from observations of Sexual maturity mating pairs. Gravid females were kept until oviposition SVL of females (n=67 preserved specimens) varied be- (1–15 days at 24 oC), before release at their capture sites. tween 178 mm and 469 mm; the smallest mature female These females were maintained individually in boxes of was 257 mm. SVL of males (n=31) varied between 160 mm polyethylene sterilized with iodine solution. Eggs were and 451 mm; the smallest mature male was 192 mm. One counted and weighed within 48 hours of oviposition, and of two immature males had an SVL of 207 mm, which incubated in humid, sterilized vermiculite at about 28 ºC. was larger than the SVL of two mature males. All males Hatchlings were counted, measured, weighed, marked and above 207 mm SVL were sexually mature. released at their mother’s capture sites after they hatched. The seasonal distribution of body size classes indicated Relative clutch mass (RCM) was calculated as the ratio that males attain sexual maturity in the first reproductive between clutch mass and female total mass (including the season after their birth (Fig. 1). The capture of small in- clutch mass) (cf. Seigel & Fitch, 1984). The relationships dividuals in December suggests that some females do between the size of eggs, hatchlings and females were not attain sexual maturity in the first reproductive season investigated using linear regression. (Fig. 1). Reproductive frequency was estimated from the pro- portion of gravid females found during the reproductive Sexual dimorphism season (cf. Plummer, 1984). Only captures from Novem- SVL of females (n=337) varied between 104 mm and ber were used because in October many females did not 490 mm, and SVL of males (n=300) varied between have well developed follicles that could be detected by 114 mm and 500 mm (Fig. 2). There was no signifi- palpation, and in December several females had already cant difference between the SVL of newborn females laid eggs. and males (n=60 ♀ and 40 ♂; x=134.9±10.9 mm and Distributions were tested for normality and homogene- 136.8±10.9 mm, respectively; t=0.85, df=98, P=0.397). ity of variances using Kolmogorov–Smirnov and Levene The mean SVL of mature females was significantly tests, respectively. All analyses used α=0.05. Mean val- higher than that of mature males (n=188 ♀ and 239 ♂; ues are presented with ±1 standard deviation. Statistical x =351.1±45.0 mm and 321.3±57.20 mm, respectively; analyses were performed with SPSS 10.0 for Windows t'=6.04, df=425, P<0.001), although individuals of both (SPSS Inc., 1999). sexes attain similar maximum SVL (Fig. 2).

220 Reproduction of Xenodon dorbignyi

Fig. 2. Relationship between tail length and snout–vent Fig. 3. Relationship between body mass and snout– length of female (circles) and male (triangles) Xenodon vent length of female (circles) and male (triangles) dorbignyi. Xenodon dorbignyi.

Males had significantly longer tails than females follicles, n=24). There was no significant difference be- in all body size classes (Fig. 2). Taking only newborns tween the mean number of eggs per clutch and the mean into consideration (n=60 ♀ and 40 ♂), the regressions number of follicles in secondary vitellogenesis per fe- of ln TL on ln SVL did not differ in slope between the male (t=0.30, df=48, P=0.976). Female SVL explained sexes (F1.96=1.37, P=0.245), but were significantly dif- 9% of the variation in the number of eggs or vitellogenic 2 ferent in their intercepts (F1.97=179.86, P<0.001); males follicles (r =0.09, F1.48=4.50, P=0.039); 24% of the varia- had proportionally longer tails than females. Considering tion in the mean mass of eggs per clutch was determined 2 mature individuals (n=188 ♀ and 238 ♂), the regres- by maternal SVL (r =0.24, F1.24=7.42, P=0.012). RCM sions had different slopes (F1.422=17.49, P<0.001). After ranged between 0.19 and 0.42 (x =0.34±0.05, n=25), and reaching maturity, the growth of the tail is proportionally in 80% of observations (n=20) was above 0.30. Mean higher in males than in females. Hatchling mass varied mass of eggs per clutch explained 67% of the variation in between 2.50 g and 4.50 g among males (x =3.44±0.47 g, SVL, and 77% of the variation in body mass of hatchlings 2 2 n=40) and between 2.50 g and 4.65 g among females (r =0.67, F1.19=38.74, P<0.001 and r =0.77, F1.19=64.37, (x =3.37±0.48 g, n=60); there were no intersexual dif- P<0.001, respectively). Maternal SVL explained 18% of ferences in slopes (F1.96=0.96, P=0.330) and intercepts the variation in SVL and body mass of hatchlings; the

(F1.97=0.03, P=0.858) when comparing regressions of regressions were, however, only marginally significant 2 2 ln body mass against ln SVL (Fig. 3). For mature indi- (r =0.18, F1.19=4.23, P=0.054 and r =0.18, F1.19=4.30, viduals collected from March to July (n=28 ♀ and 56 ♂), P=0.052, respectively). such regressions did not differ in their slopes (F1.80=0.49, P=0.488), but were significantly different with respect to their intercepts (F1.81=5.49, P=0.022); females were rela- tively heavier than males at comparable SVL (Fig. 3).

Reproductive cycle Vitellogenic follicles were recorded from August to Janu- ary (Fig. 4, Table 1). Matings were recorded in August (n=1), September (n=1), October (n=4), November (n=1) and December (n=1, Table 1). Gravid females (n=61) were found from late September to early February, and clutches (n=26) were recorded from November to February (Table 1). Hatchlings (n=100 individuals from 21 clutches) were born from early January to late April (Table 1), after in- cubation periods that lasted 58–90 days ( x =80±7 days, n=21 clutches).

Clutch size and relative mass The number of eggs varied from three to ten per clutch (x=5.3±1.6 eggs, n=26) and the number of vitellogenic Fig. 4. Seasonal variation in the diameter of the largest follicles varied from three to 12 per female (x =5.3±2.1 ovarian follicles in mature female Xenodon dorbignyi.

221 R.B. Oliveira et al.

Table 1. Seasonal occurence of vitellogenesis, matings, gravid females, oviposition and hatching of Xenodon dorbignyi. "X" represents occurrence. Numbers represent observations, with numbers of clutches in parentheses where applicable. Aug Sep Oct Nov Dec Jan Feb Mar Apr Vitellogenesis X X X X X X Matings 1 1 4 1 1 Gravid females 1 15 31 11 2 1 Oviposition 14 7 3 2 Hatching 20 (4) 55 (11) 15 (4) 10 (2)

Reproductive frequency One female was captured gravid (detected by palpation) The relative number of mature females found gravid in on 1 November 2002, and recaptured, again gravid, on 1 November in six consecutive years (1998–2003) varied January 2003. from 46.7 to 80.0% (x =65.5 %) (Table 2). Annual re- production was observed in two females (field #136 and DISCUSSION 1098) captured gravid in two consecutive reproductive seasons. Maturity and sexual dimorphism Female X. dorbignyi might produce more than one Among Squamata, larger species tend to attain maturity at clutch per reproductive season. Female MCP 11405 was a smaller proportion of the maximum size (Shine & Char- collected on 8 November 1999 and oviposited 14 days nov, 1992). For X. dorbignyi, the relative size of maturity later. On 3 December, the specimen died, containing was 0.52 and 0.38 for females and males, respectively. well developed, 10 mm long follicles. Two matings were These values are low compared to Liophis aesculapii recorded for females that had just laid eggs. On 2 No- (♀=0.74, ♂=0.59; Marques, 1996), L. poecilogyrus vember 2000, one female was found laying eggs buried (♀=0.61, ♂=0.57; Maciel, 2001), X. merremii (♀=0.42, in the sand, with four males close to her. All five indi- ♂=0.57; Jordão, 1996) and X. neuwiedii (♀=0.67, ♂=0.47; viduals were collected and put together in a terrarium, Jordão, 1996), despite the fact that these species attain where the female oviposited before mating with a male. a larger SVL than X. dorbignyi (except for male L. po- Another female, captured gravid and kept in captivity un- ecilogyrus). As a general rule, male snakes attain sexual til oviposition, was released on 25 November 2000, and maturity before females, due to their smaller reproductive was found mating the following morning. On two other costs (Parker & Plummer, 1987). occasions (6 and 15 November 1999), males were found Female snakes attain larger body size than conspecific courting gravid females who oviposited a few days later. males in the majority of species (Shine, 1993; for Xeno- dontini see Jordão, 1996; Marques, 1996; Maciel, 2001; Frota, 2005). Male and female X. dorbignyi are born with similar SVL, attain approximately the same body size at older ages and probably have similar growth patterns. Table 2. Absolute and relative numbers of mature Males usually attain equal or larger sizes than females in female Xenodon dorbignyi found gravid in November species with male combat (Shine, 1993). At present we from 1998 to 2003. have no evidence for combats in X. dorbignyi, and the lack of differences in body size reached by males and fe- Number Total number Percentage males may be due to an advantage for large males during of gravid of mature of gravid reproductive aggregations. Year females females females That males have relatively larger tails than females is 1998 5 7 71.4 common in snakes (King, 1989; Shine, 1993). In species that form reproductive aggregations, male tail length is 1999 10 14 71.4 related to reproductive success, and linked to the ability to actively remove the tail of other males from the female’s 2000 9 12 75.0 cloaca (Madsen & Shine, 1993; Shine et al., 1999). The large size of the tail in male X. dorbignyi may reflect the 2001 4 5 80.0 morphological differences related to the presence of the hemipenis described by King (1989). An advantage for 2002 7 15 46.7 males with longer tails in reproductive aggregations can also not be discarded. 2003 1 2 50.0 In many snakes, females are heavier than males of the same length (Shine, 1993), which may be a result of Total 36 55 65.5 fecundity selection. In X. dorbignyi, fecundity selection

222 Reproduction of Xenodon dorbignyi may act towards the production of larger eggs, which re- Only in two out of six years was the proportion of grav- sult in larger hatchlings. id females recorded in November equal to or lower than 50%. This is probably an underestimate, as oviposition Reproductive cycle starts in early November and the detection of pregnancy The presence of well-developed follicles in a female col- by palpation is only possible when the eggs are well de- lected in mid-August indicates that vitellogenesis begins veloped; we therefore assume that most females reproduce in July, followed by rapid follicular development (Keogh annually. Multiple clutches in the same reproductive sea- et al., 2000). Seasonal reproduction is common in tem- son have not yet been recorded for Brazilian snakes under perate snakes (Seigel & Ford, 1987). In southern Brazil, natural conditions, despite the simultaneous occurrence reproductive seasonality was recorded in all snakes, in- of developed follicles and eggs in oviducts of Xeno- cluding the Xenodontini Liophis flavifrenatus, L. jaegeri, dontini (Liophis aesculapii: Marques, 1996; L. viridis: L. miliaris, L. poecilogyrus, X. dorbignyi, X. merremii Vitt,1983; Xenodon merremii: Di-Bernardo et al.,2007; and X. neuwiedii (e.g. Leitão-de-Araújo, 1978; Pontes & Xenodon neuwiedii: Jordão, 1996), multiple clutches in Di-Bernardo, 1988; Aguiar & Di-Bernardo, 2005; Bal- captivity (L. aesculapii: Marques, 1996; L. jaegeri, L. estrin & Di-Bernardo, 2005; Di-Bernardo et al., 2007). poecilogyrus and X. merremii: Di-Bernardo, 1998), and Aseasonal reproduction or extensive vitellogenesis was individuals with follicles of three different size classes (L. verified in several species of Xenodontini in northern miliaris and X. neuwiedii: Di-Bernardo, 1998). However, Brazil (Liophis aesculapii: Marques, 1996; L. poecilogy- following Seigel & Ford (1987), the mere presence of rus: Vitt & Vangilder, 1983; Pinto & Fernandes, 2004; vitellogenic follicles does not guarantee that they become L. reginae and L. typhlus: Martins, 1994; X. merremii: eggs in the same reproductive season, and the occurrence Jordão, 1996; Vitt, 1983; X. neuwiedi: Jordão,1996; of multiple clutches in captivity may be due to higher Marques, 1998; X. severus: Dixon & Soini, 1986). Ac- food availability. Di-Bernardo et al. (2007) suggested cording to Jordão (1996) and Marques (1996), species of that multiple clutches might occur in natural conditions Xenodontini are able to reproduce continually, although when food availability is high, and the follicular devel- reproduction is constrained by environmental factors in opment rate is high enough to convert at least some of some regions. Shine (1977) suggested that the synchro- the well-developed follicles into eggs. The evidence of niszd reproductive cycles in temperate snakes are a result multiple clutches obtained from museum specimens and of temperature constraints on egg development, and also the records in captivity for Xenodontini species indicate ensure that births occur when food availability is high- the ability to produce multiple clutches. Mating soon after est. The synchronization among the reproductive cycles egg laying was recorded, as was a specimen with devel- of all oviparous snakes in Rio Grande do Sul suggests that oped follicles just after having laid eggs. Several females environmental temperature is the factor that determines that laid eggs in January and February may already have reproductive cycles in the region, although the diet of X. produced a clutch at the beginning of the reproductive dorbignyi is locally composed of anurans that may be season. abundant only for a short period (Oliveira et al., 2001). ACKNOWLEDGEMENTS Clutch size and relative mass, and reproductive frequency We are grateful to Moema Leitão de Araújo (Curator of Our study suggests that all follicles generally developed the MCN reptile collection) and Lígia Krause (at the time into eggs. The correlation between the number of eggs and of this study, Curator of the DZUFRGS reptile collection) SVL was weak, whereas egg mass was strongly related to for lending material, to DEPRC (Departamento Estadu- the female’s SVL, possibly as a result of selective forces al de Portos Rios e Canais) for providing climatic data, acting towards an increase in hatchling size rather than to Márcio Borges Martins, Ronaldo Fernandes, Mirco hatchling number. Oliveira et al. (2004) noted that preda- Solé and Sônia Cechin, for criticisms and suggestions, tion on X. dorbignyi by Athene cunicularia (burrowing to Otavio Marques, Robert Jehle and an anonymous re- owl) was biased towards smaller individuals, confirming viewer for criticisms and suggestions, to John Measey that larger hatchlings might have higher survival. and Taran Grant for review of the manuscript, to CAPES Vitt & Price (1982) demonstrated that RCM is lower (Coordenadoria de Aperfeiçoamento de Pessoal de Nível in species that depend on mobility and velocity to cap- Superior) and CNPq (Conselho Nacional de Desenvolvi- ture their prey and/or to avoid predators. Seigel & Fitch mento Científico e Tecnológico) for a doctoral fellowship (1984), however, revealed that only some species matched to RBO, to CNPq (Process # 478190/2003-4) and to this prediction. Xenodon dorbignyi is a cryptic and active FAPERGS (Fundação de Amparo à Pesquisa do Estado forager that moves slowly, feeds on inactive amphibians do Rio Grande do Sul, Process # 01/1716.4) for financial and shows elaborate defensive behaviour (Oliveira, 2001, support, and to IBAMA (Instituto Brasileiro do Meio Am- Oliveira et al., 2001; Tozetti et al., 2009). RCM values are biente e dos Recursos Naturais Renováveis) for issuing similar to, for example, members of the genus Heterodon, the licence to collect specimens in the study area (Proc- to which it is not very closely related (Zaher et al., 2009), ess IBAMA # 02001.006311/01-34). MD was partially despite morphological and ecological similarities. This financed by the Conselho Nacional de Desenvolvimento suggests that RCM is probably determined by factors re- Científico e Tecnológico (Process CNPq # 307.992/2004- lated to the species’ ecology. 7).

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